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Motility and Adhesion Through Type IV Pili in Gram-Positive Bacteria

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Motility and Adhesion Through Type IV Pili in Gram-Positive Bacteria HHS Public Access Author manuscript Author ManuscriptAuthor Manuscript Author Biochem Manuscript Author Soc Trans. Author Manuscript Author manuscript; available in PMC 2018 February 28. Published in final edited form as: Biochem Soc Trans. 2016 December 15; 44(6): 1659–1666. doi:10.1042/BST20160221. Motility and adhesion through type IV pili in Gram-positive bacteria Kurt H. Piepenbrink1 and Eric J. Sundberg1,2,3 1Institute of Human Virology, University of Maryland School of Medicine, Baltimore, MD 21201, U.S.A 2Department of Medicine, University of Maryland School of Medicine, Baltimore, MD 21201, U.S.A 3Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, U.S.A Abstract Type IV pili are hair-like bacterial surface appendages that play a role in diverse processes such as cellular adhesion, colonization, twitching motility, biofilm formation, and horizontal gene transfer. These extracellular fibers are composed exclusively or primarily of many copies of one or more pilin proteins, tightly packed in a helix so that the highly hydrophobic amino-terminus of the pilin is buried in the pilus core. Type IV pili have been characterized extensively in Gram-negative bacteria, and recent advances in high-throughput genomic sequencing have revealed that they are also widespread in Gram-positive bacteria. Here, we review the current state of knowledge of type IV pilus systems in Gram-positive bacterial species and discuss them in the broader context of eubacterial type IV pili. Introduction Pili or fimbriae are hair-like appendages present on the surface of bacterial cells. They are universally oligomeric fibers composed of protein subunits called pilins. They can be assembled noncovalently through β-strand insertion (chaperone–usher pili or the recently characterized Bacteroidia FimA family) or through subunit interactions (curli or type IV pili) or covalently through sortase linkage (cell wall-linked pili) [1–4]. In type IV pili, the pilin subunits are arranged in a repeating helical pattern. Each pilin consists of an N-terminal helical domain composed primarily of hydrophobic amino acids (bearing a strong resemblance to a transmembrane helix) and a soluble ‘headgroup’ domain. In the assembled pilus, the subunits are arranged such that the hydrophobic N-termini are in the interior of the fiber with the soluble headgroups forming the exterior [5,6]. The noncovalent association of pilin N-termini provides the energy for pilus assembly and the soluble portions are monomeric [5]. Correspondence: Eric J. Sundberg ([email protected]). Competing Interests The Authors declare that there are no competing interests associated with the manuscript. Piepenbrink and Sundberg Page 2 Type IV pili serve a variety of functions including motility along solid surfaces [7,8], Author ManuscriptAuthor Manuscript Author Manuscript Author Manuscript Author adhesion to eukaryotic host cells [9,10], microcolony/biofilm formation [11–13], and horizontal gene transfer [14]. All of these functions are dependent on one or more of three basic activities: (i) extension, lengthening the pilus through polymerization; (ii) adhesion, the ability of one or more pilus subunits to bind to target surfaces or biomolecules; and (iii) retraction, shortening the pilus through depolymerization. For example, twitching motility, across smooth, dry solid surfaces, involves all three — pili extend, bind weakly to the surface, and as the pilus is retracted, the bacterium is pulled toward the point of attachment. Type IV pili in Gram-negative bacteria have been divided historically into two classes, types IVa and IVb. This classification is based on evolutionary relationships inferred from the length of an N-terminal signal peptide (the prepilin leader sequence), which is shorter for type IVa pilins, and the identity of the first residue of the mature protein, phenylalanine for type IVa with another hydrophobic residue for type IVb. Type IVa pilins are typically smaller than their type IVb counterparts, forming thinner pilus fibers, and there is less variation in genetic organization among the type IVa pilus systems than their type IVb counterparts [4]. Functionally, type IVa pili are frequently implicated in eukaryotic cell adhesion [9,10] and horizontal gene transfer [15] and less frequently in biofilm formation [11,12], whereas type IVb pili promote bacterial self-association (i.e. microcolony formation or auto-aggregation) [16,17]. Despite the evolutionary gulf between Gram-positive and Gram-negative bacteria, many of the components in the type IV pilus system appear to be conserved; the questions before us in this review are (i) what can we learn from the differences between type IV pili in Gram- positive and Gram-negative bacteria? and (ii) how are diverse functions accomplished through the flexible molecular architecture of type IV pili? Type IV pilus biogenesis While type IV pili are composed almost entirely of repeating units of a single protein, called either simply the pilin or the major pilin, other proteins, commonly referred to as minor pilins, can be incorporated into the pilus in smaller numbers. Additionally, there are several intracellular proteins required for pilus assembly, extension, and retraction that are typically the most conserved components of type IV pilus systems. Pilin proteins The three type IV pilus systems highlighted in the figures of this review were chosen as representatives of different classes of type IV pili; Streptococcus pneumoniae R6 contains a Com operon, a DNA-uptake system found in a wide range of Gram-positive and Gram- negative bacteria [18], Clostridium difficile R20291 produces classical type IV pili similar, in some respects, to those of type IVb pilus systems [19,20], and Ruminococcus albus 8 uses a largely uncharacterized and unusual pilus system to adhere to cellulose [21,22]. Also discussed here are unique type IV pilus systems from related bacterial species Clostridium perfringens and Streptococcus sanguinis. Biochem Soc Trans. Author manuscript; available in PMC 2018 February 28. Piepenbrink and Sundberg Page 3 Figure 1A shows the putative pilin genes for C. difficile R20291, S. pneumoniae R6, and R. Author ManuscriptAuthor Manuscript Author Manuscript Author Manuscript Author albus 8. Each of these genes was identified based on three criteria: (i) the presence of a signal peptide, (ii) a recognition site for a prepilin peptidase, GFxxxE (see below), and (iii) a transmembrane-like α-helix in the predicted protein product. The known major pilin genes (pilA1 for C. difficile and R. albus, comGC for S. pneumoniae; colored orange) are the closest putative pilin genes to their common promoters, consistent with their higher expression levels. Both C. difficile and C. perfringens contain multiple clusters of type IV pilin genes as well as multiple copies of genes encoding pilus biogenesis proteins PilB, PilC, and PilM. The presence of multiple pilB genes in particular implies that Clostridia produce more than one type IV pilus or homologous secretion system, as is the case for several strains of Escherichia coli as well as S. sanguinis [23–25]. For C. difficile, only those genes predicted to be involved in the production of PilA1 pili are included in Figure 1. The genes colored blue (pilK for C. difficile and comGG for S. pneumoniae) likely encode initiator pilins that form the template upon which polymerization begins. These proteins lack a conserved glutamate residue at position 5 of the mature protein, which is thought to form a salt-bridge with the N-terminus of the previously incorporated pilin (and hence is not required for the first subunit) [26], and are much larger than their cognate major pilin proteins. Proteins with these two features can be found in most type IV pilus systems and appear analogous to GspK of the E. coli type II secretion system [27]. EGC03637.1 from R. albus 8 and BAB81985.1 from C. perfringens str. 13 are similarly large and may represent equivalent proteins. The role of the other genes encoding putative pilins, depicted in gray in Figure 1A, remains to be determined, but we expect that they can be conceptually divided into two classes: those which form a complex with the initiator pilin before the major pilin is polymerized and hence are found primarily at the tip of the pilus and those which are incorporated sporadically throughout the pilus in place of one of the major pilin subunits. The latter category, which we refer to as ‘intercalated pilins’ in Figure 1C, is only sparsely characterized at present and presumably provides no benefit in terms of stabilization; one possible function then is to provide additional adhesive activities to pili into which they are incorporated. Prepilin processing Any protein that can be incorporated into a type IV pilus is first incorporated into the plasma membrane by the hydrophobic α-helix conserved among all pilins. This insertion is dependent on a signal peptide at the N-terminus [28]. However, before extraction from the membrane and insertion into the pilus, the signal peptide must be cleaved by a prepilin peptidase (Figure 1C). Although poorly conserved, prepilin peptidase genes can be identified clearly in the genomes of C. difficile R20291, S. pneumoniae R6, and R. albus 8 as shown in Figure 1B, as well as in C. perfringens str 13 (WP_043013013.1) and S. sanguinis 2908 (CEL91498.1). Notably, all strains of C. difficile contain two genes encoding putative prepilin peptidases, one of which, pilD2, is similar to the pilD gene of C. perfringens with the other, pilD1 (which is listed in Figure 1B), being more similar to the pilD genes of Gram-negative bacteria [23]. Biochem Soc Trans. Author manuscript; available in PMC 2018 February 28. Piepenbrink and Sundberg Page 4 Pilus extension and retraction Author ManuscriptAuthor Manuscript Author Manuscript Author Manuscript Author All type IV pilus and type II secretion systems utilize cytoplasmic hexameric AAA+ family ATPases to extend the pilus or pseudopilus, respectively. These proteins are universally required for pilus biogenesis and easily identifiable by their sequence similarity.
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